Rhizosheath drought responsiveness is variety-specific and a key component of belowground plant adaptation.

Biophysicochemical rhizosheath properties play a vital role in plant drought adaptation. However, their integration into the framework of plant drought response is hampered by incomplete mechanistic understanding of their drought responsiveness and unknown linkage to intraspecific plant-soil drought reactions. Thirty-eight Zea mays varieties were grown under well-watered and drought conditions to assess the drought responsiveness of rhizosheath properties, such as soil aggregation, rhizosheath mass, net-rhizodeposition, and soil organic carbon distribution. Additionally, explanatory traits, including functional plant trait adaptations and changes in soil enzyme activities, were measured. Drought restricted soil structure formation in the rhizosheath and shifted plant-carbon from litter-derived organic matter in macroaggregates to microbially processed compounds in microaggregates. Variety-specific functional trait modifications determined variations in rhizosheath drought responsiveness. Drought responses of the plant-soil system ranged among varieties from maintaining plant-microbial interactions in the rhizosheath through accumulation of rhizodeposits, to preserving rhizosheath soil structure while increasing soil exploration through enhanced root elongation. Drought-induced alterations at the root-soil interface may hold crucial implications for ecosystem resilience in a changing climate. Our findings highlight that rhizosheath soil properties are an intrinsic component of plant drought response, emphasizing the need for a holistic concept of plant-soil systems in future research on plant drought adaptation.

Physiological recovery of tree water relations upon drought release-response of mature beech and spruce after five years of recurrent summer drought.

As climate change progresses, the frequency and duration of drought stress events are increasing. While the mechanisms of drought acclimation of trees has received considerable attention in recent years, the recovery processes remain critically understudied. We used a unique throughfall exclusion experiment in a mature temperate mixed forest consisting of the more isohydric Norway spruce and more anisohydric European beech, to study the recovery and resilience after drought release. We hypothesized that pre-dawn water potential (ΨPD) of both species will increase within 1 day after watering, while the recovery of stomatal conductance (gs) and the reversal of osmoregulation will be significantly delayed in the more isohydric spruce. Furthermore, we hypothesized that the xylem sap flow density (udaily) will not fully recover within the growing season due to the strong drought impact. After 5 years of summer drought, trees showed significantly reduced ΨPD, udaily and increased osmoregulation in leaves, but only isohydric spruce displayed increased leaf abscisic acid concentrations. In line with our hypothesis, ΨPD and gs recovered within 1 day in beech. Conversely, isohydric spruce showed delayed increases in ΨPD and gs. The delay in recovery of spruce was partially related to the replenishment of the stem water reservoir, as indicated by the missing response of udaily at the crown base compared with DBH level upon watering. However, udaily fully recovered only in the next growing season for beech and was still reduced in spruce. Nevertheless, in both species, osmotic acclimations of leaves were reversed within several weeks. While both species displayed full resilience to drought stress in water-related physiology, the recovery time was in several cases, e.g., udaily, ΨPD and gs, shorter for beech than for spruce. With future increases in the frequency of drought events under ongoing climate change, tree species that recover more quickly will be favored.

Dynamics of initial carbon allocation after drought release in mature Norway spruce-Increased belowground allocation of current photoassimilates covers only half of the carbon used for fine-root growth.

After drought events, tree recovery depends on sufficient carbon (C) allocation to the sink organs. The present study aimed to elucidate dynamics of tree-level C sink activity and allocation of recent photoassimilates (Cnew ) and stored C in c. 70-year-old Norway spruce (Picea abies) trees during a 4-week period after drought release. We conducted a continuous, whole-tree 13 C labeling in parallel with controlled watering after 5 years of experimental summer drought. The fate of Cnew to growth and CO2 efflux was tracked along branches, stems, coarse- and fine roots, ectomycorrhizae and root exudates to soil CO2 efflux after drought release. Compared with control trees, drought recovering trees showed an overall 6% lower C sink activity and 19% less allocation of Cnew to aboveground sinks, indicating a low priority for aboveground sinks during recovery. In contrast, fine-root growth in recovering trees was seven times greater than that of controls. However, only half of the C used for new fine-root growth was comprised of Cnew while the other half was supplied by stored C. For drought recovery of mature spruce trees, in addition to Cnew , stored C appears to be critical for the regeneration of the fine-root system and the associated water uptake capacity.

No xylem phenotypic plasticity in mature Picea abies and Fagus sylvatica trees after 5 years of throughfall precipitation exclusion.

Forest trees are experiencing increasing frequency and intensity of drought events with climate change. We investigated xylem and phloem traits from mature Fagus sylvatica and Picea abies trees after 5 years of complete exclusion of throughfall precipitation during the growing season. Xylem and phloem anatomy, leaf and branch biomass were analysed along top branches of ~1.5 m lenght in 5 throughfall precipitation excluded (TE) and 5 control (CO) trees of both beech and spruce. Xylem traits were analysed on wood cores extracted from the stem at breast height. In the top branches of both species, the lumen diameter (or area) of xylem and phloem conduits did not differ between TE and CO trees. At breast height, TE trees of both species produced narrower xylem rings and conduits. While allocation to branch (BM) and needle biomass (LM) did not change between TE and CO in P. abies, TE F. sylvatica trees allocated proportionally more biomass to leaves (LM) than BM compared with CO. Despite artificial drought increased the mortality in the TE plots, our results revealed no changes in both xylem and phloem anatomies, undermining the hypothesis that successful acclimation to drought would primarily involve increased resistance against air embolism.

High resilience of carbon transport in long-term drought-stressed mature Norway spruce trees within 2 weeks after drought release.

Under ongoing global climate change, drought periods are predicted to increase in frequency and intensity in the future. Under these circumstances, it is crucial for tree's survival to recover their restricted functionalities quickly after drought release. To elucidate the recovery of carbon (C) transport rates in c. 70-year-old Norway spruce (Picea abies [L.] KARST.) after 5 years of recurrent summer droughts, we conducted a continuous whole-tree 13 C labeling experiment in parallel with watering. We determined the arrival time of current photoassimilates in major C sinks by tracing the 13 C label in stem and soil CO2 efflux, and tips of living fine roots. In the first week after watering, aboveground C transport rates (CTR) from crown to trunk base were still 50% lower in previously drought-stressed trees (0.16 ± 0.01 m h-1 ) compared to controls (0.30 ± 0.06 m h-1 ). Conversely, CTR below ground, that is, from the trunk base to soil CO2 efflux were already similar between treatments (c. 0.03 m h-1 ). Two weeks after watering, aboveground C transport of previously drought-stressed trees recovered to the level of the controls. Furthermore, regrowth of water-absorbing fine roots upon watering was supported by faster incorporation of 13 C label in previously drought-stressed (within 12 ± 10 h upon arrival at trunk base) compared to control trees (73 ± 10 h). Thus, the whole-tree C transport system from the crown to soil CO2 efflux fully recovered within 2 weeks after drought release, and hence showed high resilience to recurrent summer droughts in mature Norway spruce forests. This high resilience of the C transport system is an important prerequisite for the recovery of other tree functionalities and productivity.

Friendly neighbours: Hydraulic redistribution accounts for one quarter of water used by neighbouring drought stressed tree saplings.

Hydraulic redistribution (HR) can buffer drought events of tree individuals, however, its relevance for neighbouring trees remains unclear. Here, we quantified HR to neighbouring trees in single- and mixed-species combinations. We hypothesized that uptake of HR water positively correlates with root length, number of root tips and root xylem hydraulic conductivity and that neighbours in single-species combinations receive more HR water than in phylogenetic distant mixed-species combinations. In a split-root experiment, a sapling with its roots split between two pots redistributed deuterium labelled water from a moist to a dry pot with an additional tree each. We quantified HR water received by the sapling in the dry pot for six temperate tree species. After 7 days, one quarter of the water in roots (2.1 ± 0.4 ml), stems (0.8 ± 0.2 ml) and transpiration (1.0 ± 0.3 ml) of the drought stressed sapling originated from HR. The amount of HR water transpired by the receiving plant stayed constant throughout the experiment. While the uptake of HR water increased with root length, species identity did not affect HR as saplings of Picea abies ((L.) Karst) and Fagus sylvatica (L.) in single- and mixed-species combinations received the same amount of HR water.

Close to the edge: effects of repeated severe drought on stem hydraulics and non-structural carbohydrates in European beech saplings.

Severe drought events threaten tree water transport system, productivity and survival. Woody angiosperms generally die when embolism-induced loss of hydraulic conductance (PLC) surpasses 80-90% under intense water shortage. However, the recovery capability and possible long-term carry-over effects of repeated drought events could dictate the fate of species' population under climate change scenarios. Potted saplings of European beech (Fagus sylvatica L.) were subjected to two drought cycles in two consecutive growing seasons, aiming to induce minimum leaf water potentials (Ψmd) of about -4 MPa, corresponding to hydraulic thresholds for survival of this species. In the first cycle, a well-irrigated (C) and a drought-stressed group (S) were formed, and, in the following summer, each group was divided in a well-irrigated and a drought-stressed one (four groups in total). The impact of the multiple drought events was assessed by measuring wood anatomical traits, biomass production, water relations, stem hydraulics and non-structural carbohydrate (NSC) content. We also investigated possible connections between stem hydraulics and carbon dynamics during the second drought event and following re-irrigation. S plants had lower Ψmd and maximum specific hydraulic conductivity (Ks) than C plants in the following growing season. Additionally, aboveground biomass production and leaf number were lower compared to C trees, resulting in lower water consumption. However, PLC was similar between groups, probably due to the production of new functional xylem in spring. The second drought event induced 85% PLC and promoted conversion of starch-to soluble sugars. Nevertheless, 1 week after re-irrigation, no embolism repair was observed and soluble sugars were reconverted to starch. The previous drought cycle did not influence the hydraulic performance during the second drought, and after re-irrigation S plants had 40% higher wood NSC content. Our data suggest that beech cannot recover from high embolism levels but multiple droughts might enhance stem NSC availability.

Repeated summer drought delays sugar export from the leaf and impairs phloem transport in mature beech.

Phloem sustains maintenance and growth processes through transport of sugars from source to sink organs. Under low water availability, tree functioning is impaired, i.e., growth/photosynthesis decline and phloem transport may be hindered. In a 3-year throughfall exclusion (TE) experiment on mature European beech (Fagus sylvatica L.) we conducted 13CO2 branch labeling to investigate translocation of recently fixed photoassimilates under experimental drought over 2 years (2015 and 2016). We hypothesized (H1) that mean residence time of photoassimilates in leaves (MRT) increases, whereas (H2) phloem transport velocity (Vphloem) decreases under drought. Transport of carbohydrates in the phloem was assessed via δ13C of CO2 efflux measured at two branch positions following 13CO2 labeling. Pre-dawn water potential (ΨPD) and time-integrated soil water deficit (iSWD) were used to quantify drought stress. The MRT increased by 46% from 32.1 ± 5.4 h in control (CO) to 46.9 ± 12.3 h in TE trees, supporting H1, and positively correlated (P < 0.001) with iSWD. Confirming H2, Vphloem in 2016 decreased by 47% from 20.7 ± 5.8 cm h-1 in CO to 11.0 ± 2.9 cm h-1 in TE trees and positively correlated with ΨPD (P = 0.001). We suggest that the positive correlation between MRT and iSWD is a result of the accumulation of osmolytes maintaining cell turgor in the leaves under longer drought periods. Furthermore, we propose that the positive correlation between Vphloem and ΨPD is due to a lower water uptake of phloem conduits from surrounding tissues under increasing drought leading to a higher phloem sap viscosity and lower Vphloem. The two mechanisms increasing MRT and reducing Vphloem respond differently to low water availability and impair trees' carbon translocation under drought.